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Full text of "Molecular evidence for a Jurassic origin of ants."

KURZE 



Naturwissenschaften 84. 22-23 (1997) Springer- Verlaa 1997 

Molecular Evidence for a Jurassic Origin of Ants 

R.H. Crazier. L.S. Jermiin*. M. Chiotis 

School of Genetics and Human Variation. La Trobe University. Bundoora. 
Victoria 3083. Australia 

* John Curtin School of Medical Research. Australian National University 
Canberra, ACT 2601. Australia 



The ants, a group of ecologically im- 
portant insects [1]. are commonly 
found in Oligocene and Miocene am- 
bers, whereas fossils of apparent ant- 
wasp intermediates are well known 
from the mid-Cretaceous [2]. Based 
on this record, it has become com- 
monly accepted that the ants arose no 
earlier than the late Cretaceous and 
that the adaptive radiation of extant 
ant genera took place no later than 
the start of the Tertiary [2], 

The recent discovery of Cariridris 
bipetioUmi. a Brazilian fossil from the 
Aptian of the early Cretaceous which 
has been placed in the ant subfamily 
Myrmeciinae [3] (represented today 
by the Myrmecia bulldog ants of Aus- 
tralia and nearby islands, has shown, 
however, that the ants diversified 
much earlier than previously thought, 
with Cariridris. an undoubted ant 



previously known ant-wasp intermedi- 
ates. In this review, we estimate the 
time of origin of the ant family using 
the divergences between mitochon- 
drial DNA sequences from ants of six 
subfamilies and a vespid wasp. 
We used mitochondrial cytochrome b 
sequences from Myrmecia gulosa and 
the karyotypically diverse [4] M. pilo- 
sula group [5] to calibrate the evolu- 
tionary rate of this sequence in ants. 
The evolutionary rate was calibrated 
using codon positions 1 and 2 only 
(base composition differences at posi- 
tion 3 indicate a lack of stationarity 
[6]) under the assumption that nucleo- 
tide substitutions follow Kimura's 



two-parameter model [7]. A conserva- 
tive estimate of 124.5 Ma for the age 
of Cariridris was used, this being the 
lower boundary of the Aptian, i.e., 
112-124.5 Ma ago [8]. To check the 
suitability of the data for estimating 
divergence times, we applied the rela- 
tive rate test of Wu and Li [9] (as im- 
plemented by Muse and Weir [10]). 
obtaining the results in Table 1, find- 
ing that the data do not violate the as- 
sumptions of a molecular clock. 
Using (1) this age. (2) the evolution- 
ary distances between Myrmecia spe- 
cies, and (3) the hierarchical phyloge- 
netic approach, i.e.. a method for in- 
creasing the precision in estimating 
the distance between a group of taxa 
(the M. pilosnla group) and their out- 
group (M. gulosa) by taking into ac- 
count both phylogenetic structure and 
variation in component distances [11], 
yields an estimate of the evolutionary 
rate for ants of 0.1650.023% (95% 
confidence intervals) substitutions per 
million years. 

To estimate the date of origin of the 
ants, we obtained mitochondrial DNA 
sequences homologous to those men- 
tioned above (positions 11427-12134 
in the honeybee mitochondrial gen- 
ome [12]) from five further ant sub- 
families believed to represent the 
most divergent lineages, and took the 
largest divergence value as giving the 
best estimated of the age of the 
group. This approach yields an age of 
185 36 Ma ago (95% confidence 
limits derived from the SE of the di- 
vergence estimate: Fig. 1). Similar re- 



suits follow from an analysis using 
nonsynonymous substitutions [13]. 
The larger distances to the wasp, with 
a relatively narrow spread compared 
to those between ants, indicate that 
saturation has not been a serious 
problem in this calculation. 
Our finding thus places the origin of 
the ants in the early Jurassic, at least 
70 Ma earlier than recorded by fossils 
[3], and placing the group within the 



Million years since divergence 

Fig. 1. Sequence divergences and inferred di- 
vergence times between Myrmecia groups 
(solid circle), among the ant subfamilies 
(open circles ). and between the wasp Vespida 
vitlgaris and the ant subfamilies (solid 
squares ). Divergence times were based on an 
evolutionary rate which was determined 
using the evolutionary distances in cyto- 
chrome b sequence codon positions 1 and 2 
between species groups of living M\rmecia 
bulldog ants, and the age of the fossil bull- 
dog ant Cariridris. The most ancient diver- 
gence between ant subfamilies (here between 
Leptomvrmex and Tetraponera) is taken as 



% confidence 
intervals shown (bar). The greater spread of 
distances between ant subfamilies compared 
to that between them and the wasp reflects 
variation in divergence times between ant 
subfamilies. The Myrmecia [5] and Tetrapo- 
nera (18] sequences have been published pre- 
viously: new sequences, with collection 
codes and Genbank accession numbers, are 
from Camponotus sp.. nigroaeneus gp. 
(ABZI.13. U75351), Leptom\nnex unicolor 
(ACBW.01, U75354). ! 
steini gp. (ABZI.07. tT73J52). Rhvtidooonera 



lection. Canberra 



Naturwissenschaften 84 (1997 



Springer- Verlag 1997 



rate test [10] to the sequence date discussec 



Camponotiis-Leptomynnc'x 

Cainponotus-Monoinorium 

Cuinponotus-Rlivtidnprmera 

Camponotus-Tetraponeni 

Camponotits-M\nneL'ia 

Leptom\nnex-M<momoriiun 

Leptom\nnex-Rh\tid(>pimera 

Leptomyrmex-Tetraponem 

Leptomyrmex-Mynnecia 

Monomoriitm-Rhytidoponera 

Monoinoriiim-Tftntponera 

MonoiHoriiini-Myrniecia 

Rhytidoponera-Tetraponera 

Rhytidoponera-Myrinecia 

Tetraponera-Myrmecia 



0.019679 
0.003521 
0.015599 



-0.004080 

-0.009372 

0.000535 

0.012039 

0.006811 



0.007827 
0.003423 



0.028972 
0.029811 
0.029412 
0.031200 
0.031592 
0.030166 
0.029771 
0.033361 
0.031370 
0.029053 
0.031597 
0.031735 
0.03068 1 
0.030746 
0.031660 



0.679252 
0.118116 
0.530362 
0.331156 
0.649483 
0.53645 1 
0.137061 
0.280917 
0.017050 
0.414388 
0.215555 
0.537435 
0.170410 
0.254581 
0.108114 



The Vespuhi sequence was used as the outgroup. The columns show the difference between the 
distances to the outgroup. the standard deviation of the difference between the two distances, 
and the Z-statistic. None of the values approach the significance level (Z= 1.96) and hence the 
Bonferroni correction (17] was not necessary. A larger test including an additional 14 Myrme- 
cin sequences |5] also showed no detectable departure from a molecular clock. 



era of the first hymenopteran fossils 
[14]. Such a placement suggests that 
the ants diversified more slowly than 
previously thought, and that early di- 
versification of the order Hymenop- 
tera may have been more rapid than 
previously believed. The ants thus ar- 
ose very early during the breakup of 
Pangaea [15. 16]. indicating that ma- 
jor features of current distributions 
may reflect the order of separation of 
the continents. 

We thank P. Cranston. A. Gladow. 
A. A. Hoffmann and P. Pamilo for 



helpful suggestions in the course of 
this work, S. Darby for Vespula speci- 
mens, S.O. Shattuck for ant identifi- 
cations, the Australian Research 
Council and the Ian Potter Foundation 
for research support to R.H.C., and 
the John Curtin School of Medical 
Research at the Australian National 
University for its support of L.S.J. 



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organism, in: Biology and Evolution of 
Social Insects. J. Billen ed.. Leuven: Bel- 
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Holldobler. B.. Wilson. E.O.: The Ants. 
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(1989) 

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Naturwissenschaften 84. 23-25 (1997) O Springer- Verlag 1997 

Heterogeneous Turnover of Molecular Organic 
Substances from Crop Soils as Revealed by 13 C 
Labeling at Natural Abundance with Zea mays 

Eric Lichtfouse * 



Laboratoire de Biogeochimie Isotopique. Universite Pierre et Ma 
F-75252 Paris 

Because of the recent suggestion that missing sink of atmospheric CO 2 [1J. 

the terrestrial biosphere may contain a studies on the dynamics of soil organ- 

ic carbon are of particular interest to 

* Present address: Laboratoire Sols et Envir- tr Y to understand changes in the glob- 

onnement. INRA/ENSAIA-INPL, BP 172. F- al carbon cycle [2]. Most investiga- 

54505 Vandoeuvre-les-Nancv. France tions build models that consider soil 



carbon as the sum of bulk pools of 
various turnovers [2]. However, a 
simple consideration of the huge reac- 
tivity difi'erences that exist between 
individual organic substances, such as 
lipids. amino acids, and carbohy- 
drates, strongly suggests that these 
compounds may also have signifi- 
cantly different dynamics in soils. If 
this is the case, models should take 
into account such heterogeneities at 
the molecular level. However, the 
dearth of knowledge on the dynamics 
of molecular species stems in large 
part from the extreme complexity of 
the soil medium and from the lack of 
suitable methods that allow long-term 
kinetics of organic species to be eval- 



Springer- Verlag 1997